OsCDPK24 and OsCDPK28 phosphorylate heat shock factor OsHSFA4d to orchestrate abiotic and biotic stress responses in rice

Global warming impacts crop production and increases crop disease. It is commonly known that heat stress (HS) caused by extreme high temperature induces HS responses but suppresses disease resistance in plants. However, the molecular basis of this trade-off remains largely unknown. Here, we report that OsHsfA4d shows strongest induction upon HS and pathogen infection among Heat Shock Factors (HSFs) in rice. The transcription factor OsHSFA4d enhances thermotolerance by binding to the heat shock element (HSE) in the promoter of HSP101 to activate its expression. OsHSFA4d also binds to the HSE in the first intron of Cellulose synthase-like F6 (CslF6) to promote its expression for suppressing PAMP-triggered ROS bursts and pathogenesis-related gene expression, inhibiting disease resistance. OsCDPK24 and OsCDPK28 interact with OsHSFA4d to form a complex that phosphorylates serine 146 (S146) of OsHSFA4d, thereby enhancing its DNA binding ability. HS induces the kinase activity of OsCDPK24/28 to increase the phosphorylation level of OsHSFA4d. Importantly, residues similar to S146 are conserved in OsHSFA4d orthologues across plant species, suggesting that such phosphorylation modules are widely employed to regulate abiotic and biotic stress responses in the plant kingdom. Fang et al. demonstrate that OsHSFA4d enhances thermotolerance by activating HSP101 and promoting CslF6 expression, which suppresses disease resistance. It is phosphorylated by OsCDPK24/28, increasing its DNA binding ability under heat stress. This trade-off mechanism of abiotic/biotic stress may broadly exist in plant kingdom.